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      Glyphosate does not substitute for glycine in proteins of actively dividing mammalian cells

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          Abstract

          Objectives

          Glyphosate ( N-phosphonomethyl glycine) and its commercial herbicide formulations have been shown to exert toxicity via various mechanisms. It has been asserted that glyphosate substitutes for glycine in polypeptide chains leading to protein misfolding and toxicity. However, as no direct evidence exists for glycine to glyphosate substitution in proteins, including in mammalian organisms, we tested this claim by conducting a proteomics analysis of MDA-MB-231 human breast cancer cells grown in the presence of 100 mg/L glyphosate for 6 days. Protein extracts from three treated and three untreated cell cultures were analysed as one TMT-6plex labelled sample, to highlight a specific pattern (+/+/+/−/−/−) of reporter intensities for peptides bearing true glyphosate treatment induced-post translational modifications as well as allowing an investigation of the total proteome.

          Results

          Comparative statistical analysis of global proteome changes between glyphosate treated and non-treated samples did not show significant differences. Crucially, filtering of data to focus analysis on peptides potentially bearing glycine for glyphosate replacement revealed that the TMT reporter intensity pattern of all candidates showed conclusively that they are all false discoveries, with none displaying the expected TMT pattern for such a substitution. Thus, the assertion that glyphosate substitutes for glycine in protein polypeptide chains is incorrect.

          Electronic supplementary material

          The online version of this article (10.1186/s13104-019-4534-3) contains supplementary material, which is available to authorized users.

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          Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement

          John Myers, Michael Antoniou, Bruce Blumberg … (2016)
          The broad-spectrum herbicide glyphosate (common trade name “Roundup”) was first sold to farmers in 1974. Since the late 1970s, the volume of glyphosate-based herbicides (GBHs) applied has increased approximately 100-fold. Further increases in the volume applied are likely due to more and higher rates of application in response to the widespread emergence of glyphosate-resistant weeds and new, pre-harvest, dessicant use patterns. GBHs were developed to replace or reduce reliance on herbicides causing well-documented problems associated with drift and crop damage, slipping efficacy, and human health risks. Initial industry toxicity testing suggested that GBHs posed relatively low risks to non-target species, including mammals, leading regulatory authorities worldwide to set high acceptable exposure limits. To accommodate changes in GBH use patterns associated with genetically engineered, herbicide-tolerant crops, regulators have dramatically increased tolerance levels in maize, oilseed (soybeans and canola), and alfalfa crops and related livestock feeds. Animal and epidemiology studies published in the last decade, however, point to the need for a fresh look at glyphosate toxicity. Furthermore, the World Health Organization’s International Agency for Research on Cancer recently concluded that glyphosate is “probably carcinogenic to humans.” In response to changing GBH use patterns and advances in scientific understanding of their potential hazards, we have produced a Statement of Concern drawing on emerging science relevant to the safety of GBHs. Our Statement of Concern considers current published literature describing GBH uses, mechanisms of action, toxicity in laboratory animals, and epidemiological studies. It also examines the derivation of current human safety standards. We conclude that: (1) GBHs are the most heavily applied herbicide in the world and usage continues to rise; (2) Worldwide, GBHs often contaminate drinking water sources, precipitation, and air, especially in agricultural regions; (3) The half-life of glyphosate in water and soil is longer than previously recognized; (4) Glyphosate and its metabolites are widely present in the global soybean supply; (5) Human exposures to GBHs are rising; (6) Glyphosate is now authoritatively classified as a probable human carcinogen; (7) Regulatory estimates of tolerable daily intakes for glyphosate in the United States and European Union are based on outdated science. We offer a series of recommendations related to the need for new investments in epidemiological studies, biomonitoring, and toxicology studies that draw on the principles of endocrinology to determine whether the effects of GBHs are due to endocrine disrupting activities. We suggest that common commercial formulations of GBHs should be prioritized for inclusion in government-led toxicology testing programs such as the U.S. National Toxicology Program, as well as for biomonitoring as conducted by the U.S. Centers for Disease Control and Prevention.
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            Is it time to reassess current safety standards for glyphosate-based herbicides?

            Laura Vandenberg, Bruce Blumberg, Michael Antoniou … (2017)
            Use of glyphosate-based herbicides (GBHs) increased ∼100-fold from 1974 to 2014. Additional increases are expected due to widespread emergence of glyphosate-resistant weeds, increased application of GBHs, and preharvest uses of GBHs as desiccants. Current safety assessments rely heavily on studies conducted over 30 years ago. We have considered information on GBH use, exposures, mechanisms of action, toxicity and epidemiology. Human exposures to glyphosate are rising, and a number of in vitro and in vivo studies challenge the basis for the current safety assessment of glyphosate and GBHs. We conclude that current safety standards for GBHs are outdated and may fail to protect public health or the environment. To improve safety standards, the following are urgently needed: (1) human biomonitoring for glyphosate and its metabolites; (2) prioritisation of glyphosate and GBHs for hazard assessments, including toxicological studies that use state-of-the-art approaches; (3) epidemiological studies, especially of occupationally exposed agricultural workers, pregnant women and their children and (4) evaluations of GBHs in commercially used formulations, recognising that herbicide mixtures likely have effects that are not predicted by studying glyphosate alone.
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              Evaluation of estrogen receptor alpha activation by glyphosate-based herbicide constituents

              Matthew Arno, Robin Mesnage, Alexia Phedonos … (2017)
              The safety, including the endocrine disruptive capability, of glyphosate-based herbicides (GBHs) is a matter of intense debate. We evaluated the estrogenic potential of glyphosate, commercial GBHs and polyethoxylated tallowamine adjuvants present as co-formulants in GBHs. Glyphosate (≥10,000 μg/L or 59 μM) promoted proliferation of estrogen-dependent MCF-7 human breast cancer cells. Glyphosate also increased the expression of an estrogen response element-luciferase reporter gene (ERE-luc) in T47D-KBluc cells, which was blocked by the estrogen antagonist ICI 182,780. Commercial GBH formulations or their adjuvants alone did not exhibit estrogenic effects in either assay. Transcriptomics analysis of MCF-7 cells treated with glyphosate revealed changes in gene expression reflective of hormone-induced cell proliferation but did not overlap with an ERα gene expression biomarker. Calculation of glyphosate binding energy to ERα predicts a weak and unstable interaction (-4.10 kcal mol-1) compared to estradiol (-25.79 kcal mol-1), which suggests that activation of this receptor by glyphosate is via a ligand-independent mechanism. Induction of ERE-luc expression by the PKA signalling activator IBMX shows that ERE-luc is responsive to ligand-independent activation, suggesting a possible mechanism of glyphosate-mediated activation. Our study reveals that glyphosate, but not other components present in GBHs, can activate ERα in vitro, albeit at relatively high concentrations.
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                Author and article information

                Contributors
                Michael N. Antoniou: michael.antoniou@kcl.ac.uk
                Armel Nicolas: anicolas@dcbiosciences.com
                Robin Mesnage: robin.mesnage@kcl.ac.uk
                Martina Biserni: martina.biserni@gmail.com
                Francesco V. Rao: frao@dcbiosciences.com
                Cristina Vazquez Martin: cmartin@dundeecellproducts.com
                Journal
                Journal ID (nlm-ta): BMC Res Notes
                Journal ID (iso-abbrev): BMC Res Notes
                Title: BMC Research Notes
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1756-0500
                Publication date (Electronic): 8 August 2019
                Publication date PMC-release: 8 August 2019
                Publication date Collection: 2019
                Volume: 12
                Electronic Location Identifier: 494
                Affiliations
                [1 ]ISNI 0000 0001 2322 6764, GRID grid.13097.3c, Department of Medical and Molecular Genetics, Faculty of Life Sciences & Medicine, Gene Expression and Therapy Group, , King’s College London, Guy’s Hospital, ; 8th Floor, Tower Wing, Great Maze Pond, London, SE1 9RT UK
                [2 ]DC Biosciences, James Lindsay Place, Dundee, DD1 5JJ UK
                [3 ]ISNI 0000000404312247, GRID grid.33565.36, Present Address: IST Austria Proteomics Service, ; Lab Building East, Am Campus 1, 3400 Klosterneuburg, Austria
                [4 ]Present Address: Platinum Informatics Ltd., Unit 8, The Vision Building, 20 Greenmarket, Dundee, DD1 4QB UK
                Article
                Publisher ID: 4534
                DOI: 10.1186/s13104-019-4534-3
                PMC ID: 6686468
                PubMed ID: 31395095
                SO-VID: af680b1b-354e-4c72-8e38-f32266c60c43
                Copyright © © The Author(s) 2019
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 2 May 2019
                Date accepted : 2 August 2019
                Funding
                Funded by: Sustainable Food Alliance
                Categories
                Subject: Research Note
                Custom metadata
                issue-copyright-statement © The Author(s) 2019

                ScienceOpen disciplines: Medicine
                Keywords: glyphosate,glycine,proteome
                Data availability:
                ScienceOpen disciplines: Medicine
                Keywords: glyphosate, glycine, proteome

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